FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Reproduction in domestic animals = Zuchthygiene2012; 47 Suppl 5; 31-41; doi: 10.1111/j.1439-0531.2012.02120.x

Post-mating inflammatory responses of the uterus.

Abstract: This review attempts to summarize the current knowledge on uterine inflammatory response after mating in horses, pigs and cattle. Post-mating endometritis has been extensively studied in horses as it has been considered to cause infertility. The inflammation is known to occur also in cattle, but it has not been investigated to a similar extent. There are a number of publications about mechanisms of post-mating uterine inflammation in pigs, which seem to resemble those in horses. The major focus of this review is the horse, but relevant literature is presented also on swine and cattle. Spermatozoa, seminal plasma and semen extenders play roles in the induction of inflammation. In addition, sperm numbers, concentration and viability, as well as the site of semen deposition may modulate the inflammatory response. Cytokines, polymorphonuclear leucocytes (PMN) and mononuclear cells represent the uterine inflammatory response to mating. Inflammation is the first line of defence against invasion and eliminates excess spermatozoa and bacteria. Semen deposition elicits a massive PMN invasion, followed by phagocytosis of sperm aided by the formation of neutrophil extracellular traps. Exposure of the female genital tract to semen is important also for endometrial receptivity and pre-implantation embryo development. Seminal plasma (SP) and inflammation elicit transient immune tolerance to antigens present in semen. SP contains immune-regulatory molecules that activate and control immune responses to antigens by stimulating expression of cytokines and growth factors and by initiating tissue remodelling. SP also regulates ovarian function. Effective elimination of excess sperm and inflammatory by-products and subsequent rapid return of the endometrium to the normal state is a prerequisite for pregnancy. Uterine backflow, driven by myometrial contractions and requiring a patent cervix, is an important physical tool in uterine drainage.
© 2012 Blackwell Verlag GmbH.
Get Full Text
Publication Date: 2012-08-29 PubMed ID: 22913558DOI: 10.1111/j.1439-0531.2012.02120.xGoogle Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research paper reviews the current understanding of the inflammatory response of the uterus after mating in horses, pigs, and cattle. It discusses the influence of sperm and seminal plasma on inflammation, the cells involved in the response, and the importance of timely inflammation resolution for successful pregnancy.

Post-Mating Inflammatory Response

  • Post-mating endometritis, an inflammation of the uterus after mating, is extensively studied in horses due to its potential to cause infertility.
  • This inflammation is also known to happen in cattle, but it hasn’t been researched as thoroughly.
  • Studies on pigs show similar mechanisms of post-mating uterine inflammation as observed in horses.

Role of Sperm and Seminal Plasma in Inflammation

  • Spermatozoa, the fluid carrying the sperm (seminal plasma), and semen extenders are key factors inducing inflammation.
  • The number, concentration, viability, and deposition site of sperm may influence the intensity of the inflammatory response.

Immune Cells Involved

  • Cytokines (proteins important for cell signaling), polymorphonuclear leucocytes (PMN), and mononuclear cells constitute the uterine inflammatory response after mating.
  • The inflammatory response functions to fight invasion and to eliminate excess sperm and bacteria. This is executed by a massive invasion of PMN, followed by the ingestion (phagocytosis) of sperm aided by the formation of neutrophil extracellular traps.

Semen Exposure and Immune Tolerance

  • Semen exposure is crucial not only for endometrial receptivity (preparation of the uterus for pregnancy) but also for pre-implantation embryo development.
  • Seminal plasma and the ensuing inflammation induce a temporary immune tolerance to antigens (foreign substances) present in semen.
  • Seminal plasma carries immune-regulating molecules that ensure proper immune responses to antigens, help express cytokines and growth factors, and initiate tissue remodeling.
  • Seminal plasma also regulates ovarian function.

Importance of Rapid Inflammation Resolution

  • Effective clearance of excess sperm and inflammatory byproducts and the subsequent rapid return of the uterus to a normal state is crucial for successful pregnancy.
  • Uterine backflow, a process driven by muscle contractions in the uterine wall and requiring an open cervix, is a significant physical factor aiding in uterine drainage.

Cite This Article

APA
Katila T. (2012). Post-mating inflammatory responses of the uterus. Reprod Domest Anim, 47 Suppl 5, 31-41. https://doi.org/10.1111/j.1439-0531.2012.02120.x

Publication

Reproduction in domestic animals = Zuchthygiene
ISSN: 1439-0531
NlmUniqueID: 9015668
Country: Germany
Language: English
Volume: 47 Suppl 5
Pages: 31-41

Researcher Affiliations

Katila, T
  • Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Mäntsälä, Finland. terttu.katila@helsinki.fi

MeSH Terms

  • Animals
  • Breeding
  • Cattle
  • Chemotaxis, Leukocyte / immunology
  • Copulation
  • Endometritis / etiology
  • Endometritis / immunology
  • Endometritis / veterinary
  • Female
  • Horses
  • Insemination / immunology
  • Leukocytosis / veterinary
  • Macrophages / immunology
  • Male
  • Neutrophils / immunology
  • Pregnancy
  • Semen / immunology
  • Sperm Count
  • Spermatozoa / immunology
  • Swine
  • Uterus / immunology

Citations

This article has been cited 53 times.
  1. Choudhary P, Magloire D, Hamonic G, Wilson HL. Immune responses in the uterine mucosa: clues for vaccine development in pigs. Front Immunol 2023;14:1171212.
    doi: 10.3389/fimmu.2023.1171212pubmed: 37483639google scholar: lookup
  2. Li Y, Wang H, Wang S, Zhang Q, Zhang H, Li T, Wang Q, Guo M, Feng H, Song Y, Wei G, Li J. Methylprednisolone improves the quality of liquid preserved boar spermatozoa in vitro and reduces polymorphonuclear neutrophil chemotaxis and phagocytosis. Front Vet Sci 2023;10:1177873.
    doi: 10.3389/fvets.2023.1177873pubmed: 37256001google scholar: lookup
  3. Ezz MA, Mansouri A, Akthar I, Yousef MS, Kowsar R, Miyamoto A. Hyaluronan regulates sperm-induced inflammatory response by enhancing sperm attachment to bovine endometrial epithelial cells via CD44: in-silico and in-vitro approaches. Front Endocrinol (Lausanne) 2023;14:1134868.
    doi: 10.3389/fendo.2023.1134868pubmed: 37234812google scholar: lookup
  4. Li H, Liu L, Wang J, Zhao W. The emerging role of neutrophil extracellular traps in endometritis. Front Immunol 2023;14:1153851.
    doi: 10.3389/fimmu.2023.1153851pubmed: 37033951google scholar: lookup
  5. Donnellan EM, Cormican P, Reid C, Duggan G, Stiavnicka M, Meade KG, Fair S. The transcriptomic response of bovine uterine tissue is altered in response to sperm from high- and low-fertility bulls†. Biol Reprod 2023 Jun 9;108(6):912-921.
    doi: 10.1093/biolre/ioad031pubmed: 36947086google scholar: lookup
  6. Hidalgo AI, Ulloa-Leal C, Gajardo G, López G, Carretta D, Burgos RA, Ratto M. Ovulation Induced by Intrauterine Seminal Plasma Increases Total Protein, PGE2, IL-8, and IL-1β in Uterine Fluid of Llamas (Lama glama). Animals (Basel) 2023 Feb 5;13(4).
    doi: 10.3390/ani13040554pubmed: 36830341google scholar: lookup
  7. Marey MA, Ma D, Yoshino H, Elesh IF, Zinnah MA, Fiorenza MF, Moriyasu S, Miyamoto A. Sperm induce proinflammatory responses in the uterus and peripheral blood immune cells of artificially inseminated cows. J Reprod Dev 2023 Apr 3;69(2):95-102.
    doi: 10.1262/jrd.2022-124pubmed: 36775285google scholar: lookup
  8. Alghamdi AS, Fedorka CE, Scoggin KE, Esteller-Vico A, Beatty K, Davolli G, Ball BA, Troedsson MHT. Binding of Equine Seminal Lactoferrin/Superoxide Dismutase (SOD-3) Complex Is Biased towards Dead Spermatozoa. Animals (Basel) 2022 Dec 23;13(1).
    doi: 10.3390/ani13010052pubmed: 36611662google scholar: lookup
  9. Dahlen CR, Reynolds LP, Caton JS. Selenium supplementation and pregnancy outcomes. Front Nutr 2022;9:1011850.
    doi: 10.3389/fnut.2022.1011850pubmed: 36386927google scholar: lookup
  10. Petroff MG, Nguyen SL, Ahn SH. Fetal-placental antigens and the maternal immune system: Reproductive immunology comes of age. Immunol Rev 2022 Jul;308(1):25-39.
    doi: 10.1111/imr.13090pubmed: 35643905google scholar: lookup
  11. Moya C, Rivera-Concha R, Pezo F, Uribe P, Schulz M, Sánchez R, Hermosilla C, Taubert A, Gärtner U, Zambrano F. Adverse Effects of Single Neutrophil Extracellular Trap-Derived Components on Bovine Sperm Function. Animals (Basel) 2022 May 20;12(10).
    doi: 10.3390/ani12101308pubmed: 35625154google scholar: lookup
  12. Pakravan N, Abbasi A, Hassan ZM. New Paradigm in Cell Therapy Using Sperm Head to Restore Brain Function and Structure in Animal Model of Alzheimer's Disease: Support for Boosting Constructive Inflammation vs. Anti-Inflammatory Approach. J Immunol Res 2022;2022:8343763.
    doi: 10.1155/2022/8343763pubmed: 35571563google scholar: lookup
  13. Gardela J, Ruiz-Conca M, Wright D, López-Béjar M, Martínez CA, Rodríguez-Martínez H, Álvarez-Rodríguez M. Semen Modulates Cell Proliferation and Differentiation-Related Transcripts in the Pig Peri-Ovulatory Endometrium. Biology (Basel) 2022 Apr 18;11(4).
    doi: 10.3390/biology11040616pubmed: 35453814google scholar: lookup
  14. Wang TE, Yeh LY, Kuo-Kuang Lee R, Lu CH, Yang TH, Kuo YW, Joshi R, Tsai PS, Li SH. Secretory mouse quiescin sulfhydryl oxidase 1 aggregates defected human and mouse spermatozoa in vitro and in vivo. iScience 2021 Oct 22;24(10):103167.
    doi: 10.1016/j.isci.2021.103167pubmed: 34667943google scholar: lookup
  15. Kusama K, Rashid MB, Kowsar R, Marey MA, Talukder AK, Nagaoka K, Shimada M, Khatib H, Imakawa K, Miyamoto A. Day 7 Embryos Change the Proteomics and Exosomal Micro-RNAs Content of Bovine Uterine Fluid: Involvement of Innate Immune Functions. Front Genet 2021;12:676791.
    doi: 10.3389/fgene.2021.676791pubmed: 34262596google scholar: lookup
  16. Batra V, Bhushan V, Ali SA, Sarwalia P, Pal A, Karanwal S, Solanki S, Kumaresan A, Kumar R, Datta TK. Buffalo sperm surface proteome profiling reveals an intricate relationship between innate immunity and reproduction. BMC Genomics 2021 Jun 26;22(1):480.
    doi: 10.1186/s12864-021-07640-zpubmed: 34174811google scholar: lookup
  17. Schjenken JE, Sharkey DJ, Green ES, Chan HY, Matias RA, Moldenhauer LM, Robertson SA. Sperm modulate uterine immune parameters relevant to embryo implantation and reproductive success in mice. Commun Biol 2021 May 14;4(1):572.
    doi: 10.1038/s42003-021-02038-9pubmed: 33990675google scholar: lookup
  18. Bidarimath M, Lingegowda H, Miller JE, Koti M, Tayade C. Insights Into Extracellular Vesicle/Exosome and miRNA Mediated Bi-Directional Communication During Porcine Pregnancy. Front Vet Sci 2021;8:654064.
    doi: 10.3389/fvets.2021.654064pubmed: 33937376google scholar: lookup
  19. Elesh IF, Marey MA, Zinnah MA, Akthar I, Kawai T, Naim F, Goda W, Rawash ARA, Sasaki M, Shimada M, Miyamoto A. Peptidoglycan Switches Off the TLR2-Mediated Sperm Recognition and Triggers Sperm Localization in the Bovine Endometrium. Front Immunol 2020;11:619408.
    doi: 10.3389/fimmu.2020.619408pubmed: 33643300google scholar: lookup
  20. Wojtysiak K, Ryszka W, Stefaniak T, Król J, Kozdrowski R. Changes in the Secretion of Anti-Inflammatory Cytokines and Acute-Phase Proteins in the Uterus after Artificial Insemination in the Mare. Animals (Basel) 2020 Dec 19;10(12).
    doi: 10.3390/ani10122438pubmed: 33352707google scholar: lookup
  21. Gardela J, Jauregi-Miguel A, Martinez CA, Rodríguez-Martinez H, López-Béjar M, Álvarez-Rodríguez M. Semen Modulates Inflammation and Angiogenesis in the Reproductive Tract of Female Rabbits. Animals (Basel) 2020 Nov 25;10(12).
    doi: 10.3390/ani10122207pubmed: 33255666google scholar: lookup
  22. Batra V, Dagar K, Nayak S, Kumaresan A, Kumar R, Datta TK. A Higher Abundance of O-Linked Glycans Confers a Selective Advantage to High Fertile Buffalo Spermatozoa for Immune-Evasion From Neutrophils. Front Immunol 2020;11:1928.
    doi: 10.3389/fimmu.2020.01928pubmed: 32983120google scholar: lookup
  23. Marey MA, Aboul Ezz M, Akthar I, Yousef MS, Imakawa K, Shimada M, Miyamoto A. Sensing sperm via maternal immune system: a potential mechanism for controlling microenvironment for fertility in the cow. J Anim Sci 2020 Aug 18;98(Suppl 1):S88-S95.
    doi: 10.1093/jas/skaa147pubmed: 32810249google scholar: lookup
  24. Omeljaniuk WJ, Jabłońska E, Garley M, Pryczynicz A, Ratajczak-Wrona W, Socha K, Borawska MH, Charkiewicz AE. Biomarkers of neutrophil extracellular traps (NETs) and nitric oxide-(NO)-dependent oxidative stress in women who miscarried. Sci Rep 2020 Aug 4;10(1):13088.
    doi: 10.1038/s41598-020-70106-xpubmed: 32753622google scholar: lookup
  25. Gardela J, Ruiz-Conca M, Martinez CA, Wright D, López-Béjar M, Rodriguez-Martinez H, Alvarez-Rodriguez M. The Expression of Cold-Inducible RNA-Binding Protein mRNA in Sow Genital Tract Is Modulated by Natural Mating, But Not by Seminal Plasma. Int J Mol Sci 2020 Jul 27;21(15).
    doi: 10.3390/ijms21155333pubmed: 32727091google scholar: lookup
  26. Zhu C, Hu W, Zhao M, Huang MY, Cheng HZ, He JP, Liu JL. The Pre-Implantation Embryo Induces Uterine Inflammatory Reaction in Mice. Reprod Sci 2021 Jan;28(1):60-68.
    doi: 10.1007/s43032-020-00259-7pubmed: 32651899google scholar: lookup
  27. Hamonic G, Pasternak JA, Ng SH, Fourie KR, Simko OM, Deluco B, Wilson HL. Assessment of Immunological Response and Impacts on Fertility Following Intrauterine Vaccination Delivered to Swine in an Artificial Insemination Dose. Front Immunol 2020;11:1015.
    doi: 10.3389/fimmu.2020.01015pubmed: 32536924google scholar: lookup
  28. Chastant S, Saint-Dizier M. Inflammation: friend or foe of bovine reproduction?. Anim Reprod 2019 Oct 24;16(3):539-547.
    doi: 10.21451/1984-3143-AR2019-0057pubmed: 32435296google scholar: lookup
  29. Bruno V, Corrado G, Baci D, Chiofalo B, Carosi MA, Ronchetti L, Piccione E, Albini A, Noonan DM, Piaggio G, Vizza E. Endometrial Cancer Immune Escape Mechanisms: Let Us Learn From the Fetal-Maternal Interface. Front Oncol 2020;10:156.
    doi: 10.3389/fonc.2020.00156pubmed: 32226771google scholar: lookup
  30. Badrakh D, Yanagawa Y, Nagano M, Katagiri S. Effect of seminal plasma infusion into the vagina on the normalization of endometrial epidermal growth factor concentrations and fertility in repeat breeder dairy cows. J Reprod Dev 2020 Apr 10;66(2):149-154.
    doi: 10.1262/jrd.2019-148pubmed: 31996487google scholar: lookup
  31. Stadtmauer DJ, Wagner GP. Cooperative inflammation: The recruitment of inflammatory signaling in marsupial and eutherian pregnancy. J Reprod Immunol 2020 Feb;137:102626.
    doi: 10.1016/j.jri.2019.102626pubmed: 31783286google scholar: lookup
  32. Sereshki N, Andalib A, Ghahiri A, Mehrabian F, Sherkat R, Rezaei A, Wilkinson D. The expression of human leukocyte antigen by human ejaculated spermatozoa. Mol Genet Genomic Med 2019 Dec;7(12):e1005.
    doi: 10.1002/mgg3.1005pubmed: 31625276google scholar: lookup
  33. Tecle E, Reynoso HS, Wang R, Gagneux P. The female reproductive tract contains multiple innate sialic acid-binding immunoglobulin-like lectins (Siglecs) that facilitate sperm survival. J Biol Chem 2019 Aug 2;294(31):11910-11919.
    doi: 10.1074/jbc.RA119.008729pubmed: 31201275google scholar: lookup
  34. Ezz MA, Marey MA, Elweza AE, Kawai T, Heppelmann M, Pfarrer C, Balboula AZ, Montaser A, Imakawa K, Zaabel SM, Shimada M, Miyamoto A. TLR2/4 signaling pathway mediates sperm-induced inflammation in bovine endometrial epithelial cells in vitro. PLoS One 2019;14(4):e0214516.
    doi: 10.1371/journal.pone.0214516pubmed: 30995239google scholar: lookup
  35. Alhussien MN, Dang AK. Potential roles of neutrophils in maintaining the health and productivity of dairy cows during various physiological and physiopathological conditions: a review. Immunol Res 2019 Feb;67(1):21-38.
    doi: 10.1007/s12026-019-9064-5pubmed: 30644032google scholar: lookup
  36. Tríbulo P, Balzano-Nogueira L, Conesa A, Siqueira LG, Hansen PJ. Changes in the uterine metabolome of the cow during the first 7 days after estrus. Mol Reprod Dev 2019 Jan;86(1):75-87.
    doi: 10.1002/mrd.23082pubmed: 30383328google scholar: lookup
  37. Miller DJ. Review: The epic journey of sperm through the female reproductive tract. Animal 2018 Jun;12(s1):s110-s120.
    doi: 10.1017/S1751731118000526pubmed: 29551099google scholar: lookup
  38. Raad G, Hazzouri M, Bottini S, Trabucchi M, Azoury J, Grandjean V. Paternal obesity: how bad is it for sperm quality and progeny health?. Basic Clin Androl 2017;27:20.
    doi: 10.1186/s12610-017-0064-9pubmed: 29123667google scholar: lookup
  39. Tecle E, Gagneux P. Sugar-coated sperm: Unraveling the functions of the mammalian sperm glycocalyx. Mol Reprod Dev 2015 Sep;82(9):635-50.
    doi: 10.1002/mrd.22500pubmed: 26061344google scholar: lookup
  40. Aitken RJ, Baker MA, Nixon B. Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress?. Asian J Androl 2015 Jul-Aug;17(4):633-9.
    doi: 10.4103/1008-682X.153850pubmed: 25999358google scholar: lookup
  41. Lawler C, Milho R, May JS, Stevenson PG. Rhadinovirus host entry by co-operative infection. PLoS Pathog 2015 Mar;11(3):e1004761.
    doi: 10.1371/journal.ppat.1004761pubmed: 25790477google scholar: lookup
  42. Hahn S, Giaglis S, Hoesli I, Hasler P. Neutrophil NETs in reproduction: from infertility to preeclampsia and the possibility of fetal loss. Front Immunol 2012;3:362.
    doi: 10.3389/fimmu.2012.00362pubmed: 23205021google scholar: lookup
  43. Alfatlawy HJ. Microbial profile of post-breeding endometritis in Arabian mares from the Al-Hira District, Iraq. Open Vet J 2025;15(8):3670-3676.
    doi: 10.5455/OVJ.2025.v15.i8.30pubmed: 41035988google scholar: lookup
  44. Beckers KF, Liu CC, Gomes VCL, Schulz CJ, Childers GW, Fedorka CE, Sones JL. Effects of Intra-uterine Ceftiofur on the Equine Uterine Microbiome. Vet Sci 2025 Aug 30;12(9).
    doi: 10.3390/vetsci12090837pubmed: 41012762google scholar: lookup
  45. Nash DM, Giles JL. Uterine inflammation and lessons from large animal models of endometritis. Nat Rev Immunol 2025 Dec;25(12):934-946.
    doi: 10.1038/s41577-025-01200-2pubmed: 40696155google scholar: lookup
  46. Chan HY, Schjenken JE, Sharkey DJ, Robertson SA. Assessing Seminal Fluid Interaction with Female Reproductive Tract Tissues: In Vivo and In Vitro Models for Mouse. Methods Mol Biol 2025;2897:649-662.
    doi: 10.1007/978-1-0716-4406-5_44pubmed: 40202667google scholar: lookup
  47. Chera JS, Gaur V, Kumar A, Josan F, Patel A, Yadav S, Karanwal S, Verma P, Verma V, Kumar S, Bairagi AK, Kamal S, Datta TK, Kumar R. Surface N- or O-linked glycans on bovine spermatozoa play minimal role in evading macrophage mediated phagocytosis. Front Vet Sci 2025;12:1550100.
    doi: 10.3389/fvets.2025.1550100pubmed: 40196804google scholar: lookup
  48. Reot L, Adapen C, Cannou C, Nunez N, Lakoum S, Pimienta C, Lacroix L, Binois O, Frydman N, Nugeyre MT, Le Grand R, Menu E. Seminal plasma inhibits Chlamydia trachomatis infection in vitro, and may have consequences on mucosal immunity. Sci Rep 2024 Sep 9;14(1):21050.
    doi: 10.1038/s41598-024-71499-9pubmed: 39251689google scholar: lookup
  49. Batra V, Dagar K, Diwakar MP, Kumaresan A, Kumar R, Datta TK. The proteomic landscape of sperm surface deciphers its maturational and functional aspects in buffalo. Front Physiol 2024;15:1413817.
    doi: 10.3389/fphys.2024.1413817pubmed: 39005499google scholar: lookup
  50. León M, Moya C, Rivera-Concha R, Pezo F, Uribe P, Schulz M, Sánchez R, Taubert A, Hermosilla C, Zambrano F. Extrusion of Neutrophil Extracellular Traps (NETs) Negatively Impacts Canine Sperm Functions: Implications in Reproductive Failure. Int J Mol Sci 2024 Jun 5;25(11).
    doi: 10.3390/ijms25116216pubmed: 38892404google scholar: lookup
  51. Kilama J, Dahlen CR, Reynolds LP, Amat S. Contribution of the seminal microbiome to paternal programming. Biol Reprod 2024 Aug 15;111(2):242-268.
    doi: 10.1093/biolre/ioae068pubmed: 38696371google scholar: lookup
  52. Brennan PLR, Purdy S, Bacon SJ. Intra-horn insemination in the alpaca Vicugna pacos: Copulatory wounding and deep sperm deposition. PLoS One 2024;19(4):e0295882.
    doi: 10.1371/journal.pone.0295882pubmed: 38630763google scholar: lookup
  53. Mouncey R, Arango-Sabogal JC, Rathbone P, Scott CJ, de Mestre AM. Prevalence of Microbial Isolates Cultured from Endometrial Swab Samples Collected from United Kingdom Thoroughbred Mares from 2014 to 2020. Vet Sci 2024 Feb 9;11(2).
    doi: 10.3390/vetsci11020082pubmed: 38393100google scholar: lookup
Subscribe to our newsletter
Join 99,911 horse owners like you who receive our email updates on horse health and nutrition.